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Key message: OsMYB1 negatively mediates rice resistance to brown planthopper and rice blight. Additionally, OsMYB1 interacts with OsSPL14 and antagonizes its function by oppositely regulating downstream resistance-related genes. In their natural habitats, plants are concurrently attacked by different biotic factors. Xanthomonas oryzae pv. oryzae (Xoo) is a pathogen that severely deteriorates rice yield and quality, and brown planthopper (BPH; Nilaparvata lugens) is a rice specific insect pest with the damage topping other pathogens. Although genes for respective resistance to BPH and Xoo have been widely reported, few studies pay attention to simultaneous resistance to both. In this study, we identified a MYB transcription factor, OsMYB1, which exhibited diverse transcriptional regulatory capabilities and a negative regulatory role in resistance to both BPH and Xoo. Biochemical and genetic analysis proved OsMYB1 to be a TF that could interact with OsSPL14, a positive regulator of rice resistance to Xoo. OsSPL14 mutants showed increased sensitivity to BPH, suggesting that OsSPL14 is contrary to OsMYB1 in regulating rice resistance to these two biotic stresses. Consistently, OsMYB1 and OsSPL14 displayed opposite functions in regulating defense-related genes. OsMYB1 can form transcription regulation complexes with repressor OsJAZs instead of co-repressor TOPLESS to possibly realize its transcriptional repression function. Taken together, we concluded that two interacting TFs in rice, OsMYB1 and OsSPL14, played antagonistic roles in regulating resistance to BPH and Xoo. [ABSTRACT FROM AUTHOR]

Summary: Terpene synthases (TPSs) are key enzymes in terpenoids synthesis of plants and play crucial roles in regulating plant defence against pests and diseases. Here, we report the functional characterization of OsTPS19 and OsTPS20, which were upregulated by the attack of brown planthopper (BPH). BPH female adults performed concentration‐dependent behavioural responses to (S)‐limonene showing preference behaviour at low concentrations and avoidance behaviour at high concentrations. Overexpression lines of OsTPS19 and OsTPS20, which emitted higher amounts of the monoterpene (S)‐limonene, decreased the hatching rate of BPH eggs, reduced the lesion length of sheath blight caused by Rhizoctonia solani and bacterial blight caused by Xanthomonas oryzae. While knockout lines of OsTPS19 and OsTPS20, which emitted lower amounts of (S)‐limonene, were more susceptible to these pathogens. Overexpression of OsTPS19 and OsTPS20 in rice plants had adverse effects on the incidence of BPH, rice blast, and sheath blight in the field and had no significant impacts on rice yield traits. OsTPS19 and OsTPS20 were found to be involved in fine‐tuning the emission of (S)‐limonene in rice plants and play an important role in defence against both BPH and rice pathogens. [ABSTRACT FROM AUTHOR]

[Display omitted] • Alanine was a key biomarker of BPH adaptation to resistant rice variety IR36. • ALT-mediated alanine transfer to pyruvate was necessary and sufficient for the adaptation. • The high level of ALT activity rendered more energy reserves in the adapted BPH population. • Higher energy reserves improved detoxification and ecological fitness recovery in BPH consuming IR36-resistant rice. During the adaptation to host plant resistance, herbivorous insects faced the challenge of overcoming plant defenses while ensuring their own development and reproductive success. To achieve this, a strategic allocation of energy resources for detoxification and ecological fitness maintenance became essential. This study aimed to elucidate the intricate energy allocation mechanisms involved in herbivore adaptation that are currently poorly understood. The rice Oryza sativa and its monophagous pest, the brown planthopper (BPH), Nilaparvata lugens were used as a model system. An integrated analysis of metabolomes and transcriptomes from different BPH populations were conducted to identify the biomarkers. RNA interference of key genes and exogenous injection of key metabolites were performed to validate the function of biomarkers. We found that alanine was one of the key biomarkers of BPH adaptation to resistant rice variety IR36. We also found that alanine flow determined the adaptation of BPH to IR36 rice. The alanine aminotransferase (ALT)-mediated alanine transfer to pyruvate was necessary and sufficient for the adaptation. This pathway may be conserved, at least to some extent, in BPH adaptation to multiple rice cultivars with different resistance genes. More importantly, ALT-mediated alanine metabolism is the foundation of downstream energy resource allocation for the adaptation. The adapted BPH population exhibited a significantly higher level of energy reserves in the fat body and ovary when fed with IR36 rice, compared to the unadapted population. This rendered the elevated detoxification in the adapted BPH and their ecological fitness recovery. Overall, our findings demonstrated the crucial role of ALT-mediated alanine metabolism in energy allocation during the adaptation to resistant rice in BPH. This will provide novel knowledge regarding the co-evolutionary mechanisms between herbivores and their host plants. [ABSTRACT FROM AUTHOR]

Background: The endocycle can generate cells referred to as 'polyploid'. Fizzy‐related protein (Fzr) plays an important role in driving the mitosis‐to‐endocycle transition. The brown planthopper (BPH), Nilaparvata lugens (Stål), a serious insect pest, feeds exclusively on rice. However, polyploidy and its regulatory mechanisms are poorly understood in BPH. Results: Here, we found that the ploidy levels of follicles H (FH) and accessory gland (AG) significantly increased with BPH age when examining the polyploidy of FH and AG of salivary glands. Fzr was identified as an important regulator for polyploidy in BPH salivary gland. Knockdown of Fzr resulted in a decrease in cell size and DNA content in nymph salivary glands. Fzr knockdown transcriptionally upregulated cyclin‐dependent kinase 1 (CDK1), CDK2, cyclin A (CycA) and CycB, and downregulated CycD, CycE, Myc and mini‐chromosome maintenance protein 2‐7 (MCM2‐7). Phenotypically, Fzr knockdown significantly suppressed salivary protein production, feeding and survival in BPH nymphs. Conclusion: Our results show that BPH salivary glands exhibit obvious polyploidy, and Fzr positively regulates the endocycle in nymph salivary gland. These findings provide clues for the study of the regulatory mechanisms of insect polyploidy. © 2024 Society of Chemical Industry. [ABSTRACT FROM AUTHOR]

Introduction: During the adaptation to host plant resistance, herbivorous insects faced the challenge of overcoming plant defenses while ensuring their own development and reproductive success. To achieve this, a strategic allocation of energy resources for detoxification and ecological fitness maintenance became essential. Objective: This study aimed to elucidate the intricate energy allocation mechanisms involved in herbivore adaptation that are currently poorly understood. Methods: The rice Oryza sativa and its monophagous pest, the brown planthopper (BPH), Nilaparvata lugens were used as a model system. An integrated analysis of metabolomes and transcriptomes from different BPH populations were conducted to identify the biomarkers. RNA interference of key genes and exogenous injection of key metabolites were performed to validate the function of biomarkers. Results: We found that alanine was one of the key biomarkers of BPH adaptation to resistant rice variety IR36. We also found that alanine flow determined the adaptation of BPH to IR36 rice. The alanine aminotransferase (ALT)-mediated alanine transfer to pyruvate was necessary and sufficient for the adaptation. This pathway may be conserved, at least to some extent, in BPH adaptation to multiple rice cultivars with different resistance genes. More importantly, ALT-mediated alanine metabolism is the foundation of downstream energy resource allocation for the adaptation. The adapted BPH population exhibited a significantly higher level of energy reserves in the fat body and ovary when fed with IR36 rice, compared to the unadapted population. This rendered the elevated detoxification in the adapted BPH and their ecological fitness recovery. Conclusion: Overall, our findings demonstrated the crucial role of ALT-mediated alanine metabolism in energy allocation during the adaptation to resistant rice in BPH. This will provide novel knowledge regarding the co-evolutionary mechanisms between herbivores and their host plants.

The effectiveness and sustainable application of insecticides are severely threatened by the rapid evolution of resistance in agricultural pests. Recent research indicates that odorant binding proteins (OBPs) may be involved in facilitating insecticide resistance, while the specific mechanisms remain poorly understood. Herein, 11 OBPs were identified from Nilaparvata lugens. Among them, OBP5 exhibited high and specific expression in the head, and showed constitutive overexpression in the chlorpyrifos-resistant strain. Knockdown of OBP5 notably restored susceptibility to chlorpyrifos in N. lugens , while overexpression of OBP5 in Escherichia coli significantly enhanced bacterial tolerance to chlorpyrifos. Fluorescence competitive binding assay confirmed the strong binding affinities of OBP5 to chlorpyrifos and its active metabolite chlorpyrifos-oxon. Molecular docking studies proposed a critical interacting amino acid (Lys147) in the binding site, which was further validated by comparative binding studies between wildtype OBP5 and the mutated protein OBP5K147A. Furthermore, Lim1β that also presented overexpression pattern in the resistant strain, was found to regulate expression of OBP5 through a dual-luciferase reporter assay. Our findings demonstrate that the overexpression of OBP5 contributes to chlorpyrifos resistance by binding and sequestering the insecticides, shedding light on the sequestration resistance mechanism conferred by OBPs and offering potential targets for resistance management. • High-affinity binding of OBP5 to the insecticides confers chlorpyrifos resistance in N. lugens. • A critical interacting residue (Lys147) within the binding site was identified. • Lim1β promotes chlorpyrifos resistance by transcriptionally regulating OBP5. • Resistance can be reduced by inhibiting the interaction between OBP5 and insecticides. [ABSTRACT FROM AUTHOR]